<p>Stocking native herbivores such as the Caribbean King Crab (<i>Maguimithrax spinosissimus</i>) is a promising strategy for controlling macroalgal proliferation and supporting coral reef restoration. In the Florida Keys, saltwater quarries have been proposed as semi-wild mariculture sites for producing crabs for large-scale stocking, but this approach requires understanding population dynamics to avoid genetic incompatibilities between wild and quarry sources. Here, we used population genomics to assess genetic diversity, structure, selection, connectivity, and effective population size in crab populations from the wild and quarries. Additionally, we applied ecological niche modeling to investigate whether <i>M. spinosissimus</i> is predicted to remain in the Florida Keys under different climate scenarios. Using 3,677 genome-wide SNPs from 82 individuals across 9 sites (6 wild, 4 quarry), we show that crabs in quarries retain genomic diversity comparable to crabs from wild locations, exhibit no detectable genomic structure among all populations, and have stable recent effective population sizes. Connectivity analyses reveal migration between all locations, including migrants from quarries into the wild. Migration patterns are mainly from the south to the north, consistent with regional oceanographic patterns. However, adaptive loci unique to crabs collected in one of the quarries, suggests potential local adaptation in at least one location. Ecological niche models indicate that the Florida Keys may persist as a suitable habitat for <i>M. spinosissimus</i> considering projections until 2100. These findings support the genetic viability of quarry-based mariculture as part of the large-scale stocking of <i>M. spinosissimus</i> for coral reef restoration that is consistent with guidelines for global conservation translocations.</p>